Diversification, adaptation, and community assembly of the American oaks (Quercus), a model clade for integrating ecology and evolution
Abstract
Summary
Ecologists and evolutionary biologists are concerned with explaining the diversity and composition of the natural world and are aware of the inextricable linkages between ecological and evolutionary processes that maintain the Earth's life support systems. Yet examination of these linkages remains challenging due to the contrasting nature of focal systems and research approaches. Model clades provide a critical means to integrate ecology and evolution, as illustrated by the oaks (genus Quercus), an important model clade, given their ecological dominance, remarkable diversity, and growing phylogenetic, genomic, and ecological data resources. Studies of the clade reveal that their history of sympatric parallel adaptive radiation continues to influence community assembly today, highlighting questions on the nature and extent of coexistence mechanisms. Flexible phenology and hydraulic traits, despite evolutionary stasis, may have enabled adaptation to a wide range of environments within and across species, contributing to their high abundance and diversity. The oaks offer fundamental insights at the intersection of ecology and evolution on the role of diversification in community assembly processes, on the importance of flexibility in key functional traits in adapting to new environments, on factors contributing to persistence of long-lived organisms, and on evolutionary legacies that influence ecosystem function.
I. Model clades for the study and integration of ecology and evolution
A model system, in general, is one that has features that make it particularly good for advancing science in a certain direction. Model organisms are species that have been widely studied, usually because they are easy to maintain and breed in a laboratory setting, or they have advantages for examining particular aspects of biology experimentally; for example, gene function. Model clades (Knapp et al., 2004; Buell, 2009), by contrast, are lineages of organisms that allow us to advance understanding of particular concepts, such as the role of biogeographic history in community assembly. A model clade for integrating ecology and evolution must have features that allow us to understand how evolutionary processes bear on ecological processes, and vice versa. For understanding the importance of evolution for ecosystem processes, it is advantageous if the clade also plays an important ecosystem role. Model clades are well-studied lineages that have accumulated important phylogenetic, genetic, and functional trait or ecological data; they frequently include one or more species with significant genomic resources (Supporting Information Table S1). As a consequence, model clades have the potential to contribute to conservation of biodiversity and ecosystems through enhanced understanding of the influence of the deep past on current mechanisms of community assembly and the likely ecological and evolutionary responses of organisms to changing environments (Fig. 1a).
Plant ecologists interested in comparative approaches rarely focus on clades, tending instead to work at broad phylogenetic scales. Important advances have been made at these large scales in examining the evolutionary mechanisms for trait coordination along major axes of life history variation, such as the leaf economic spectrum (Ackerly & Reich, 1999; Wright et al., 2004; Moles et al., 2005; Kerkhoff et al., 2006; Donovan et al., 2011), freezing adaptation (Zanne et al., 2014, 2018), or mechanisms of seed dormancy (Willis et al., 2014). Yet working within highly resolved lineages is often critical to deciphering the ecological causes and direction of evolutionary shifts, given that evolutionary processes occur at smaller scales where species do not exhibit the extreme phenotypes observed across the entire evolutionary tree (Scoffoni et al., 2016). Importantly, at smaller evolutionary scales, a large proportion of the species can be sampled, phylogenetic information tends to be highly resolved, and functional trait measurements can be carefully obtained – generating insights that may not emerge at broad phylogenetic scales.
Using clade-based approaches, evolutionary ecologists are poised to test ecological theories about adaptive evolution, such as those related to plant defense, as examined in milkweeds (Asclepias) (Agrawal & Fishbein, 2008) or leaf photosynthetic function across light environments, as in lobeliads (Montgomery & Givnish, 2008; Givnish & Montgomery, 2014). Studies within the well-resolved Viburnum or Helianthus (sunflower) clades, for example, have shown that coordination of leaf economic spectrum traits and adaptations to environmental niches may depend more on integrated whole plant processes and allocation patterns than leaf-level trade-offs (Edwards et al., 2014; Mason & Donovan, 2015). Within the legume family, species were sufficiently sampled and assessed to determine that evolution of nondormancy in seeds is coupled to seed size and length of the growing season, likely a consequence of ecological trade-offs in carbon gain and predation risk (Rubio de Casas et al., 2017). At the scale of the grass family (Poaceae), a more nuanced understanding of the adaptive significance of photosynthetic pathways emerged compared with prior nonphylogenetic approaches (Edwards & Still, 2008). Clade-based approaches with high-density species sampling (Table S1) thus provide a means to understand the evolutionary basis for functional adaptations to the environment. Patterns observed at narrow phylogenetic scales can subsequently be tested at broader phylogenetic scales, where ecological and phenotypic data are more sparsely sampled.
Model clades can also bridge the gap between micro- and macroevolutionary processes that impact both population-level and ecosystem-level processes. The case has been made to start with a genetic model organism and expand to its relatives to uncover the genetic mechanisms that underlie eco-evolutionary dynamics (Pigliucci, 2002). However, a relatively small number of model organism- or clade-based studies focus on ecologically dominant species or approach eco-evolutionary questions at the scale of ecosystems (Edwards et al., 2010). Thus, ecological inferences from microevolutionary experimental work or macroevolutionary research may not address core ecological questions, particularly those concerning large-scale ecosystem functions. To make inferences about ecosystem processes, it can be advantageous to focus on ecological dominants even though they may have less experimentally convenient life histories. Genetic and genomic resources are increasingly being developed for species within lineages that include ecological dominants, such as the pines, the figs, the grasses, the eucalypts, and the oaks, among others (Table S1). As these resources continue to be developed and combined with phylogenetic and densely sampled trait information within lineages, model clades will serve an increasingly important role in addressing ecological questions that require understanding of micro- and macroevolutionary processes.
II. Oaks: an important model clade
From an ecological perspective, the oaks are an important model clade because they are ecological dominants inhabiting five continents; they have extraordinary diversity and abundance in North America and Mesoamerica (Nixon, 1993; Valencia, 2004; Kappelle, 2006; Rodríguez-Correa et al., 2015; Hipp et al., 2018), as well as in Eurasia (Nixon, 1997; Manos & Stanford, 2001; Manos et al., 2001; Li et al., 2004; Denk et al., 2012; Deng et al., 2018). Nixon (1997) called Quercus ‘the most important woody genus in the Northern Hemisphere’. Forest inventory data from both the USA and Mexico reveal that oaks have the highest biomass and species diversity of forest tree genera in those two countries (Cavender-Bares, 2016; Fig. 1b–e). The oaks comprise c. 20% and 29% of the total aboveground biomass in forests surveyed in the continental USA and in Mexico, respectively, with 91 species in the USA and Canada, 172 species in Mexico (Table S2), and over 260 total species in the Americas, out of over 400 species in the genus globally (Nixon, 1997, 2006; Hipp et al., 2014, 2018). As a consequence, oaks are major contributors to ecosystem function in Northern Hemisphere temperate forest systems. They provide habitat and food – due to production of acorns, leaves, and wood – for other trophic levels, including birds, squirrels, and numerous insects, which in turn provide food for many other kinds of wildlife. Their associations with ectomycorrhizal (ECM) and other fungi influence microbial composition and impact nutrient cycling and ecosystem function (Dickie et al., 2007; Nguyen et al., 2016; Cheeke et al., 2017).
As a lineage, oaks occupy a range of habitats and are ecologically diverse, which has made them the subject of considerable ecological research. They are generally characterized as drought tolerant (Whittaker & Niering, 1975; Abrams, 1990; Osuna et al., 2015), as a consequence of deep rooting and hydraulic architecture (Cavender-Bares & Bazzaz, 2000; Cavender-Bares et al., 2007; Limousin et al., 2010; Barbeta et al., 2015; Feng et al., 2017; Matheny et al., 2017; Fallon & Cavender-Bares, 2018; Skelton et al., 2018), but cover a range of elevations and climates in North America (Fig. 2; Cavender-Bares et al., 2018), Mesoamerica (Poulos et al., 2007; Aguilar-Romero et al., 2017), and Europe (Infante et al., 2003; Aranda et al., 2005), including lowland, riparian, and coastal habitats (Williams et al., 1999; Kurtz et al., 2013). The capacity of many oak species to withstand fire or resprout from above- or belowground tissues after fire (Myers, 1990; Abrams, 1992; Jackson et al., 1999; Cavender-Bares et al., 2004b; Cavender-Bares & Reich, 2012; Schwilk et al., 2016) is responsible for the once-widespread oak savanna biomes of the US Midwest (Abrams, 1992; Peterson & Reich, 2008) that until recently occupied nearly a third of the continental USA (Packard & Mutel, 1997). As major components of temperate, Mediterranean, and high-elevation tropical forests and savanna ecosystems in the Northern Hemisphere, oaks contribute to human well-being through provisioning of food, wood products, and fuel, and regulation of climate, hydrology, coastal protection, and air quality (Kroeger et al., 2014).
From an evolutionary perspective, oaks are an important model clade because they allow study of introgression in relation to species boundaries and adaptive processes and serve as a representative system in which to examine how long-lived species persist, given fluctuating selection. Questions related to selection processes have more frequently been addressed in short-lived species. Oaks have been described as the worst case scenario of the biological species concept given their propensity for interspecific gene flow (Coyne & Orr, 2004); however, genetic exchange between species is increasingly understood as the norm in biology rather than the exception (Pennisi, 2016), with abundant examples among plants, including within other well-studied model clades; for example, Helianthus (Rieseberg & Carney, 1998), Ficus (Wei et al., 2014), and Eucalyptus (Field et al., 2010). Oaks have repeatedly been found to maintain species coherence, despite introgression (Van Valen, 1976; Craft & Ashley, 2010; Gailing & Curtu, 2014; Cavender-Bares et al., 2015; Eaton et al., 2015). They have a tractable and consistently diploid genome that has been mapped and sequenced (Durand et al., 2010; Hipp et al., 2013; Pereira-Leal et al., 2014; Plomion et al., 2016, 2018; Sork et al., 2016a), and genome-wide methods for reconstructing the evolutionary history of the group are well established (Hipp et al., 2014; McVay et al., 2017). A well-resolved and dated phylogeny for the monophyletic American oak lineage is now available (Hipp et al., 2018). Genomic resources are rapidly being established for individual species within the oaks, characterizing important functional genes that are critical to environmental variation (Petit et al., 2013; Lesur et al., 2015; Gugger et al., 2016; Konar et al., 2016; Sork et al., 2016b; Plomion et al., 2018). As such, the oaks can provide critical insights linking the biogeographic past and current assembly processes that impact ecosystem functions and services that contribute to human well-being (Cavender-Bares, 2016; Cavender-Bares et al., 2016a, 2018; Cannon et al., 2018). Finally, there is a large and increasing number of studies focused on population level processes within the oaks (Sork et al., 1993; Cavender-Bares, 2007; Ramírez-Valiente et al., 2011, 2015, 2017, 2018; Koehler et al., 2012; Hampe et al., 2013; Homolka et al., 2013; Platt et al., 2015; Firmat et al., 2017; Ramírez-Valiente & Cavender-Bares, 2017). These studies reveal that oaks are an important system for understanding the roles of gene flow, adaptation, and plasticity in the persistence of populations of long-lived organisms, which tend to face more variable environments and fluctuating selection over their lifespan than short-lived organisms do.
III. Insights from the history of the American oaks for understanding community assembly and ecosystem dominance
1. Sympatric parallel diversification of the oaks
A defining feature of the oaks in the Americas is their history of sympatric parallel diversification (Hipp et al., 2018), which I argue has far-reaching consequences for community assembly and ecological dominance of the oaks. The timing of diversification is associated with major changes in the Earth's climate. Climatic cooling and drying from the middle Eocene (c. 35 million yr ago, Ma) onward (Zachos et al., 2001) has been hypothesized to have created ecological opportunity in North America through local extinction of many incumbent species (Prothero, 2009) as tropical tree taxa contracted to lower latitudes (Graham, 1999, 2011). Two major oak lineages – red oaks (section Lobatae) and white oaks (section Quercus) – colonized and radiated sympatrically and in parallel into the temperate zone on either side of the Rocky Mountains, marking a major shift in the diversity and composition of North America (Hipp et al., 2018; Fig. 2). Both of these groups, which are deciduous or have variable leaf habits, radiated with nearly equal diversity and extent. Starting c. 35 Ma, these lineages diversified rapidly (Crepet & Nixon, 1989) along with limited diversification within two much smaller evergreen or subevergreen lineages (eastern live oaks, Quercus section Virentes, and western golden cup oaks, Quercus section Protobalanus). All four lineages are inferred to have developed by 30 Ma (Crepet & Nixon, 1989). By 20 Ma, the oaks accelerated their speciation rate as they extended into Mexico with the rise in volcanic activity that created three important mountain chains and provided elevation gradients across which the oaks diversified. In Mexico, the white oak and red oak clades exhibited 54% and 85% increases in their diversification rates, respectively, relative to rates north of Mexico (Hipp et al., 2018).
Adaptive radiation theory is relevant to explaining why the oaks expanded across the continent relatively rapidly during the cooling and drying starting in the Eocene. According to theory, the proliferation of an initial ancestral species into multiple descendant species and the divergence of these species to adapt to an array of different ecological conditions (Givnish & Sytsma, 1997; Stroud & Losos, 2016) requires that ancestral species have geographical and evolutionary access to ecological opportunity. Ecological opportunity in this context is ‘the availability of ecologically accessible resources that may be evolutionarily exploited’ (Stroud & Losos, 2016), either through extinction of competitors or the evolution of phenotypes that allow lineages to take advantage of resources in previously unoccupied habitats or niche space (Simpson, 1953; Schluter, 1996, 2000; Givnish & Montgomery, 2014). In the oaks, both were likely relevant. The evolvability (Ramírez-Valiente & Cavender-Bares, 2017) and plasticity (Hernández-Calderón et al., 2013; Firmat et al., 2017) of bud break timing and leaf phenology in oaks can be linked to flexible leaf abscission and prevalent deciduousness to avoid winter and seasonal drought, discussed further in Section V. These attributes likely gave them fitness advantages in changing climates and across environmental gradients in the newly created temperate zone.
The American oaks depart from many other classic adaptive radiations, in that the two major lineages diversified in sympatry. Ecological coexistence mechanisms, discussed later in this section, may have been crucial to the ability of the major oak lineages to diversify and assemble in communities sympatrically and may help explain why oaks occur at high species density relative to other lineages. The relatively rapid rate of expansion and accumulation of high diversity and abundance of oaks in North America may have preempted expansion of other lineages (Cavender-Bares et al., 2016a), providing a hypothesis for the prevalence of oaks in North America (Fig. 1b–e). Their prevalence, in turn, shapes ecosystem functions in North American temperate and high-elevation forests, as a consequence of conserved functional traits that may be uncoupled from local sorting and selection pressures.
2. High ecological diversity and repeated trade-offs across gradients are linked to sympatric parallel adaptive radiation
The imprint of sympatric parallel adaptive radiation of the oaks on the North American continent (Fig. 2) is evident at local spatial scales (Fig. 3). In Florida, oak diversity is exceptionally high (17 sympatric species in northern Florida, 26 species in the state) despite the lack of major elevation gradients (Cavender-Bares et al., 2006). Repeated functional and ecological diversity of the oaks within multiple lineages can be seen even in this circumscribed region. In northern Florida, two major lineages of oaks – the red oaks (section Lobatae) and the white oaks (section Quercus) plus the live oaks (section Virentes), which together form a monophyletic lineage – occur across the same gradients of soil moisture, fertility, and fire regime. Species are differentiated within lineages by suites of functional traits that show correlated evolution and adaptation to contrasting habitats (Cavender-Bares et al., 2004b; Fig. 3). These oaks show trade-offs in hydraulic traits associated with growth rates and drought tolerance that are coupled to hydrologic gradients (Cavender-Bares & Holbrook, 2001; Reich et al., 2003; Cavender-Bares et al., 2004b). They also show trade-offs in rhizome resprouting ability and bark thickness in response to fire, allowing species to partition fire regimes that differ in frequency and severity. Investment in bark increases aboveground survival during fire, particularly for juveniles. Investment in belowground carbohydrate storage and capacity to resprout from rhizomes allows recovery after fire, particularly when fire is quite severe (Myers, 1990; Schwilk et al., 2013).
Echoing the imprint of sympatric parallel adaptive radiation evident in Florida, red and white oaks in the Chiricahua Mountains of southern Arizona both partition an elevation gradient through physiological and phenological mechanisms (Fallon & Cavender-Bares, 2018). As a consequence, species in different sections (red and white) have overlapping niche distributions, whereas species within a section do not. Zonation patterns of oaks in this system are well explained by species differences in phenology and leaf capacitance, with species showing a trade-off between drought avoidance, on the one hand, and drought tolerance through rapid desiccation recovery, on the other hand (Fallon & Cavender-Bares, 2018).
Adaptive differentiation and local sorting among sympatric species is a pattern found across gradients throughout the American oaks. In eight common oak species of sky island mountain ranges in west Texas, bark allocation strategies vary among species with contrasting habitat preferences for wetter or drier sites; species from drier sites, with presumably greater fire frequency, invest in thicker bark (Schwilk et al., 2013), and the degree of desiccation avoidance varies with microhabit preferences (Schwilk et al., 2016). Across rainfall and aridity gradients in California (Skelton et al., 2018) and in Michoacán, Mexico (Aguilar-Romero et al., 2017), trade-offs between traits linked to xylem vulnerability, xylem hydraulic transport capacity, and drought avoidance have allowed species to partition the abiotic environment. Oak species from more arid regions have greater resistance to embolism (Skelton et al., 2018) and/or tend to abscise a greater proportion of leaves during the dry season, allowing them to avoid dry-season water stress, whereas those in more mesic regions with less severe dry seasons show less deciduousness and xylem that is more resistant to embolism (Aguilar-Romero et al., 2017). In Sierra del Carmen in Coahuila, Mexico, two arid species partition altitudinal gradients through physiological and growth mechanisms that are associated with trade-offs in growth rate and drought tolerance (Poulos et al., 2007).
More broadly, repeated variation in form and function in the oaks (Tucker, 1974) is evident in multiple lineages related to their habitats across precipitation and moisture gradients (Bahari et al., 1985; Kaproth & Cavender-Bares, 2016; Aguilar-Romero et al., 2017; Figs 2, 3), across fire gradients (Myers, 1990; Jackson et al., 1999; Cavender-Bares et al., 2004b; Cavender-Bares & Reich, 2012; Schwilk et al., 2013), elevation (Poulos et al., 2007; Schwilk et al., 2016; Fallon & Cavender-Bares, 2018), temperature gradients (Koehler et al., 2012), and successional gradients (Monk, 1968; Petit et al., 2004; Lagache et al., 2014). Ecological diversification across climatic gradients is well documented (Cavender-Bares et al., 2018; Hipp et al., 2018). For example, climate of origin is highly predictive of freezing vulnerability across the oaks, with shifts in leaf lifespan associated with vulnerability to freezing embolism (Cavender-Bares & Holbrook, 2001; Cavender-Bares et al., 2005) and photoprotection under chilling conditions (Cavender-Bares et al., 1999). Shifts in phenology have thus been critical both within and across species in adapting to temperature and water-availability gradients. They may also be important for species coexistence if contrasting phenological patterns allow temporal partitioning in light capture and access to belowground resources (Damesin et al., 1998).
Based on the aforementioned discussion, I hypothesize that oaks show high species turnover across environments (beta diversity) as well has high richness within communities (alpha diversity) because (1) multiple lineages have adaptively radiated, sympatrically, into a diversity of ecological habitats associated with variation in life-history strategies along stress tolerance–growth-rate trade-off axes; and (2) these distinct oak lineages, as well as phenologically differentiated species within lineages, are able to coexist through ecological mechanisms.
Evidence for (2) remains circumstantial, although the patterns of community structure that lead to it are compelling. Local diversity of oaks is nonrandom with respect to lineage. In northern Florida, close relatives co-occur less than expected by chance in local communities (Cavender-Bares et al., 2004a). Yet, within a given habitat, representatives from different lineages share similar phenotypes and adaptations to fire, soil moisture (Fig. 4e,f), and soil fertility (Cavender-Bares et al., 2004b). At the continental scale, distinct oak lineages consistently co-occur within communities more than expected at random (Cavender-Bares et al., 2018). Analysis of the US Forest Service Forest Inventory Analysis data in gridded plots across the USA within naturally assembled forests revealed that red and white oaks co-occur more often than expected and that there is a generalized pattern of phylogenetic overdispersion across most of the USA (Fig. 2b). Yet functional traits within communities are more similar than expected (Fig. 2c; Cavender-Bares et al., 2018). These patterns can be explained, in part, by convergent evolution in functional traits along life-history trade-off axes and in ecological niches, coupled with local environmental sorting processes (Cavender-Bares et al., 2004b, 2018; Fig. 2b–e). The diversification process that gave rise to convergence in oak species climatic niches and functional traits (Cavender-Bares et al., 2018; Hipp et al., 2018) provides a first explanation for both local- and continental-scale patterns of phylogenetic and trait community structure. Trade-offs between stress tolerance and growth-related traits are frequently associated with the abiotic environment and often mediated by phenology, leaf lifespan, and leaf desiccation avoidance, tolerance, and recovery strategies, as discussed earlier. Yet, niche convergence, alone, is unlikely the full explanation, and ecological mechanisms that allow distantly related oaks to coexist must also play a role.
3. Coexistence mechanisms
Ecological mechanisms that promote long-term coexistence of multiple oak species – through niche partitioning that reduces competition, positive interactions (facilitation) between co-occurring species that enhance establishment or growth, or reduced enemy pressure from specialized pests and pathogens – are hypothesized to have been critical in permitting sympatric radiation of two oak lineages (Cavender-Bares et al., 2004a, 2018). Yet these mechanisms remain largely untested. The repeated co-occurrence of different lineages and greater phylogenetic distance between co-occurring oaks than expected at random is indicative of mechanisms of complementarity among distant relatives. The intriguing evidence I review here, that distant relatives likely have mechanisms for coexisting with each other, remains circumstantial, making this line of questioning an important area for continued investigation.
Long-term coexistence may be promoted both by mechanisms that allow species to partition resources spatially or temporally and by resource and fitness benefits gained by having neighbors with particular attributes. Co-occurring oaks may facilitate (or benefit) each other more than has been recognized (Callaway et al., 2002). Shade and fine-root dynamics of incumbent oaks may facilitate colonization of other oak species by preventing grasses from establishing (Callaway et al., 1991; Callaway & Davis, 1998) or by enhancing soil conditions (Chavez-Vergara et al., 2015). For example, oak species with low nutrient resorption in leaves may improve soil fertility, benefitting oaks with high nutrient resorption. This appears to be the case in two broadly distributed and co-occurring Mexican oaks, Quercus deserticola and Quercus castanea. When Q. deserticola (which has higher leaf longevity but lower foliar nutrient resorption) and Q. castanea (shorter longevity but higher nutrient resorption) occur together in mixed stands, soil fertility increases compared with monotypic stands of Q. castanea. Quercus deserticola produces more nutrient-rich litter with higher nitrogen concentration, enhancing microbial activity in the forest floor litter and soil fertility to the benefit of Q. castanea (Chavez-Vergara et al., 2015).
The promotion of ECM symbionts may be a related mechanism. Distantly related oak species tend to share a proportion of their ECM symbionts (Desai et al., 2016) despite significant differentiation in ECM communities among distantly related oak hosts (Cavender-Bares et al., 2009a). ECM symbionts enhance growth of oak seedlings and likely allow them to persist in nutrient-poor soils by mobilization of various nitrogen and phosphorus forms from organic soil layers (Berman & Bledsoe, 1998; Kayama & Yamanaka, 2016). There is evidence that ECM mutualists enhance the ability of oaks to colonize new niches (Yguel et al., 2014). Once oaks establish, they may promote colonization by other oak species, but also allow them to partition soil resources spatially. The influence of leaf traits on the microbial community, through impacts on soil nutrient dynamics, may thus facilitate colonization of new sites or reduce competition through niche partitioning at fine spatial scales, or both (Aponte et al., 2013). An exciting and expanding area of study is the role of contrasting litter traits – associated with leaf longevity and nutrient resorption efficiency – in driving microbial processes belowground that may promote complementarity.
4. Pests and pathogens
Experiments and observations with both fungal pathogens and insects (Yguel et al., 2011) indicate that the co-occurrence of distantly related plant hosts reduces enemy pressure (Webb et al., 2006; Parker et al., 2015). Red and white oaks show differential susceptibility to fungal pathogens, including oak wilt (Juzwik et al., 2011) and sudden oak death (Garbelotto & Hayden, 2012), and to insect herbivores (e.g. gold-spotted oak borer, Venette et al., 2015). Moreover, herbivory patterns in oaks are predicted by phylogenetic relationships (Pearse & Hipp, 2009). As a consequence, co-occurrence of distant relatives may be expected to reduce the diversity of individuals susceptible to the same pests or pathogens, thereby reducing density-dependent mortality (Cavender-Bares et al., 2004a). Nevertheless, these outcomes have not yet been demonstrated.
5. Introgression, incomplete reproductive isolation, and adaptation
In addition to ecological mechanisms that may contribute to coexistence of distantly related oak species and to observed patterns of phylogenetic overdispersion in local communities, introgression may also play a role. The well-documented hybridization and introgression in the oaks (Whittemore & Schaal, 1991; Curtu et al., 2007; Aldrich & Cavender-Bares, 2011; Gugger & Cavender-Bares, 2013; Gailing & Curtu, 2014; Song et al., 2015; McVay et al., 2017) have a suite of evolutionary and ecological consequences, including shaping community assembly and structure. Coexistence of distant relatives, or lack of coexistence of close relatives, may be linked to reproductive isolating mechanisms (Cavender-Bares et al., 2009b). Without reproductive isolation, coexistence of distinct species cannot be maintained because introgression can cause species to merge over time (Petit et al., 2004), eliminating their co-occurrence (Losos, 1990; Levin, 2006; Pollock et al., 2015), and potentially contributing to the observed patterns of overdispersion. In contrast, functional divergences between close relatives that allow them to occupy contrasting habitats likely limit gene flow between species (Klein et al., 2016), particularly if contrasting environments promote assortative mating, such as in sympatric live oaks in the southeastern USA, discussed in Section IV (Cavender-Bares & Pahlich, 2009). Empirical and theoretical evidence indicates that the likelihood of hybridization is impacted both by community structure and by demographic factors that influence pollen limitation (Klein et al., 2016). Introgression also has other ecological consequences related to community assembly. Differentiation in seed and pollen dispersal among closely related European white oaks coupled with asymmetric introgression have been shown to be important in colonizing new habitats and in successional processes (Petit et al., 2004; Lagache et al., 2013).
Beyond potential influences on community assembly, the tendency for oaks to hybridize and introgress may also have been important in increasing genetic diversity (Valencia-Cuevas et al., 2014) and rapidly transferring adaptive alleles between species (Lexer et al., 2004; Khodwekar & Gailing, 2017). The role of horizontal gene transfer is increasingly recognized as an important factor in the ability of long-lived organisms to adapt to novel or changing environments (Lexer et al., 2004; Cannon & Lerdau, 2015; Cannon & Scher, 2017). Such processes may have facilitated the adaptation of populations to new environments during the process of radiation across the continent.
How might introgression have allowed adaptation? Oak biologists currently speculate that introgression is critical to adaptation. Cannon & Lerdau (2015), for example, propose that interspecific gene flow can play a critical role in avoiding extinction by transfer of adaptative alleles. They discuss the concept of the syngameon, in which species participate in genomic exchange through incomplete reproductive isolation, and propose that it provides selective advantages. A requirement for the syngameon to function is a conserved genomic structure and ploidy level among the interfertile species, which is met within the oaks (Cannon & Scher, 2017). Despite widespread hybridization in oaks, Cannon & Scher (2017) emphasize that hybridization does not lead to a ‘melting pot’. Genome-wide sequencing shows species coherence in oaks (Fig. 4a,b), even when they occur in sympatry and gene flow is evident (Hipp et al., 2014, 2018; Cavender-Bares et al., 2015; Eaton et al., 2015). Numerous studies using nuclear DNA markers – including microsatellites, random amplification of polymorphic DNA markers, or low-copy nuclear genes – present similar evidence (Craft et al., 2002; González-Rodríguez et al., 2004, 2005; Curtu et al., 2007; Cavender-Bares & Pahlich, 2009; Craft & Ashley, 2010; Holtken et al., 2012; Zhang et al., 2015). By contrast, chloroplast DNA, which is maternally inherited (Dumolin et al., 1995), typically shows extensive introgression (Whittemore & Schaal, 1991), and haploptypes are shared across species (Fig. 4c).
6. Evolutionary legacy effects on ecosystem function
The biogeographic history and the climatic and environmental conditions in which species evolved have a lasting influence on ecosystems through multiple mechanisms that influence community assembly and drive ecosystem processes (Fig. 1a). One mechanism is through phylogenetic conservatism of traits that evolved in one environmental context and persist in another as lineages expand and migrate to novel environments or experience climatic changes. I present two examples, which may serve to motivate further study and prompt large-scale quantitative analyses of evolutionary legacy effects across lineages. In the first, drought tolerance and deep rooting – both conserved ancestral traits of oaks – have direct ecosystem consequences in terms of forest productivity and stress resistance, even in mesic forests where many commonly occurring plant species are not particularly drought tolerant. During a decadal-scale drought in a red oak (Quercus rubra)-dominated forest in Central Massachusetts, mature oak trees maintained canopy photosynthetic rates that were only slightly reduced compared with those under nonstress conditions, while shallow-rooted yellow birch (Betula papyrifera) showed large-scale leaf wilting and leaf abscission (Cavender-Bares & Bazzaz, 2000). The small decline in photosynthetic rate of Q. rubra corresponded closely to the small decrease in gross ecosystem exchange of CO2 as determined from eddy correlation measurements in the same years. Had the forest been composed of birch, it would have shown considerable loss of productivity (Waring et al., 1996; Cavender-Bares & Bazzaz, 2004).
In the second example, tropical live oak (Quercus oleoides)-dominated ecosystems within seasonally dry tropical forests of Guanacaste, Costa Rica, show distinct ecosystem functions compared with adjacent communities as a consequence of conserved traits that likely evolved in less seasonal environments. Q. oleoides arrived at its southern range limit in Costa Rica in the seasonal dry forest region during the Middle Pleistocene (Cavender-Bares et al., 2011), perhaps through long-distance dispersal. The species can likely persist through the long dry season given its deep roots and high leaf hydraulic resistance (Cavender-Bares et al., 2007). Most seasonally dry tropical trees that occur in the same region have drought deciduous leaves (Klemens et al., 2011). The canopies of the live oaks, however, are evergreen (or subevergreen, whereby new and old leaves exchange during a brief period of time) – a conserved trait within the Virentes that is hypothesized to have evolved under mild climates (Cavender-Bares et al., 2015; Hipp et al., 2018). The foliage holds moisture during the dry season (Brodribb et al., 2003; Brodribb & Holbrook, 2006; Ramírez-Valiente & Cavender-Bares, 2017; Ramírez-Valiente et al., 2017), influencing local temperature and impacting the microclimate, water balance, and carbon dynamics where the oaks occur. In contrast to Q. oleoides, most dry forest species also have dormant seeds and arbuscular mycorrhizae. Seeds of live oaks are desiccation intolerant (Klemens et al., 2011; Center et al., 2016), and their high nutritional reserves provide food for numerous animals in the dry season. They also form ECM associations, which influence nutrient dynamics (Desai et al., 2016). Both traits are phylogenetically conserved in oaks. The constellation of traits that tropical live oaks have retained from their ancestry make them functional outliers in the tropical dry forest. Thus, relative to other forest types, lowland Q. oleoides forests have very different trophic interactions and ecosystem functions (Kissing & Powers, 2010) – a consequences of phylogenetic legacy effects.
Evolutionary priority effects are another mechanism by which the deep past influences current ecosystem function. I return to my earlier hypothesis that particular ecosystem functions of oak-dominated forests in North America may be understood as attributable to evolutionary legacies rather than to adaptations or acclimations to current climate and geology (see also Cavender-Bares et al., 2016b). To summarize the logic, the sympatric parallel diversification of the oaks occurred because of ecological opportunity at a particular time in Earth's history, and the ability to adapt to a wide range of habitats in multiple lineages simultaneously. Adaptation may have been aided by horizontal gene transfer through the syngameon, while high oak species diversity locally was promoted by ecological coexistence mechanisms. Widespread habitat colonization, through adaptive radiation into a range of ecological niches, and species packing through coexistence of multiple lineages may have preempted the radiation of other lineages that were slower to arrive or diversify. These factors together may help explain the high diversity, abundance, and widespread distribution of the oaks in the Americas. Given their dominance in many ecosystems, the particular phylogenetically conserved attributes of the oaks that set them apart from other sympatric lineages have a large influence on ecosystem functions. These attributes include, for example, litter quality and ECM fungal associations that influence nutrient cycling, deep rooting that influences hydrology, high wood density that influences productivity, and acorn production, secondary compounds, and leaf chemistry that influence other trophic levels, which in turn have ecosystem consequences. These ecosystem functions are not necessarily tightly coupled to or predicted from the climatic or geologic setting where oaks occur and would shift if other clades came to dominate. Ecosystem function, then, may be as much a consequence of the biogeographic and evolutionary history of this important clade than of other environmental factors. The potential importance of evolutionary legacies on ecosystem function is one insight that emerges from ecological and evolutionary study of a single model clade. Detailed study of the contrasting histories of other model clades can help substantiate or illuminate the importance of historical processes on ecosystem function relative to other factors, such as the abiotic environment.
IV. Bridging the gap between micro- and macroevolutionary processes relevant to ecology
Bridging the gap between populations and communities – and between micro- and macrevolutionary processes – requires operating at still smaller evolutionary scales, such as within individual species or small lineages. It is at this scale that the genetic mechanisms that explain macroevolutionary processes are most tractably studied and at which genetic and ecological information is most relevant to conservation. Oaks remain a useful model clade at this scale, particularly for understanding adaptive and neutral evolutionary processes in long-lived organisms. Oaks have been well studied in terms of the mechanisms of speciation (Ortego et al., 2015; Rodríguez-Correa et al., 2015, 2017), adaptive differentiation among populations (Sork et al., 2016b; Cavender-Bares & Ramírez-Valiente, 2017; Ramírez-Valiente et al., 2017, 2018), and factors that contribute to persistence in the context of environmental change (Saenz-Romero et al., 2017). New genomic tools (Lesur et al., 2015; Plomion et al., 2016) make long-standing questions in this realm more feasible to address. The large range sizes of many oaks allows comparison of factors that may influence population genetic structure, adaptive differentiation (Ramírez-Valiente et al., 2015, 2017), response to contrasting environments (Saenz-Romero et al., 2017), and barriers to gene flow (Rodríguez-Correa et al., 2015). However, the potential consequences of their genetic variation for ecosystem function, seen in other model systems (e.g. Populus, Schweitzer et al., 2012), remain largely uninvestigated in oaks.
1. Phylogeographic history, climatic stability, and speciation mechanisms at small evolutionary scales
We have used the live oaks (section Virentes), a small lineage (seven species, Fig. 5) within the larger American oak clade, to examine microevolutionary patterns and processes, particularly linked to vicariance mechanisms and to adaptive differentiation and selection in relation to habitat and climate. The Virentes are estimated to have emerged from 11 Ma (8.4–14.1 Ma; Cavender-Bares et al., 2015) to 15.4 Ma (14.2–18.1 Ma; Hipp et al., 2018) as an evergreen or subevergreen lineage restricted to low elevations and mild climates, which nevertheless spans the tropical–temperate divide in North America, Mesoamerica, and the Caribbean. Within Virentes, the Nicaraguan Depression, the Sea of Cortez, isolation on the Cuban island, and the dry lowland region between southern Texas and northern Mexico have served as major barriers to gene flow that have influenced population genetic structure (Fig. 4) and speciation, as documented in a series of studies on this lineage (Cavender-Bares et al., 2011, 2015; Gugger & Cavender-Bares, 2013; Eaton et al., 2015).
Signatures of vicariance and allopatric speciation predominate in the Virentes, but there are instances where sympatric speciation may have been likely (Cavender-Bares et al., 2015). For example, when sister taxa are sympatric, as in the case of Quercus virginiana and Quercus geminata, isolation by time appears to be a critical mechanism that maintains species coherence and could have led to speciation (Cavender-Bares & Pahlich, 2009). Q. virginiana, which occurs on more mesic sites, flowers nearly 2 weeks earlier than Q. geminata, which occurs on xeric and deep, sandy soils. The wetter environment may support earlier flowering before the spring rains arrive, and assortative mating due to flowering time differences appears to be critical in limiting gene flow between them. At northern latitudes, where the season length is shorter and flowering time separation is condensed, introgression is greater (Cavender-Bares & Pahlich, 2009).
Because the Virentes span a wide latitudinal gradient from the mid-Atlantic coast in the USA (state of Virginia) to northwestern Costa Rica (province of Guanacaste), it is possible to compare the phylogeographic history and population genetic structure of species across tropical and temperate zones. Long-term climate stability, which varies across this divide, is considered a critical factor driving genetic diversity and gene flow and may have influenced population genetic structure in these species. For example, the widespread tropical species Q. oleoides harbors higher genetic diversity (greater number of effective alleles and higher heterozygocity based on nuclear simple sequence repeat frequencies) and reveals fewer genetic breaks among populations (determined from Monmonier's maximum difference algorithm for genetic distances) – consistent with long-term climatic stability – than the widespread temperate species Q. virginiana. The latter shows evidence of major vicariance events and bottlenecks associated with glaciation and sea level rise (Cavender-Bares et al., 2011). The role of paleoclimate in influencing patterns of genetic diversity, population genetic structure, and speciation is an ongoing area of investigation (Ortego et al., 2015; Rodríguez-Correa et al., 2015; Rodríguez-Correa et al., 2017). Higher genetic diversity in oaks across Mexico (Rodríguez-Correa et al., 2017) than in oaks found in the northwestern USA (Marsico et al., 2009) or in Europe (Petit et al., 2002), but similar to California (Grivet et al., 2008), may be partially attributed to higher climatic stability as well as greater interspecific gene flow and complex migration patterns in Mesoamerica and California relative to temperate North America or Europe. Nevertheless, although glaciation cycles would have had less drastic impacts on vegetation in Mesoamerica than in North America, climate in Mesoamerica may not have been as stable as previously thought (Correa-Metrio et al., 2012).
2. Adaptive differentiation and local adaptation as mechanisms of long-term persistence
Limits to gene flow influence population genetic structure and speciation but do not answer how adaptive differentiation and local adaptation occur in the course of speciation (Gugger et al., 2016; Sork et al., 2016b). Nor do they address whether local adaptation is a primary mechanism underlying the persistence of populations, given that long-lived species incur fluctuating and unpredictable environments throughout the course of their lifespan. A long-standing question in evolutionary ecology is the extent to which species are comprised of a series of locally adapted populations or represent broadly adapted populations (Etterson, 2008). Local adaptation – whereby populations have higher fitness locally compared with foreign populations but lower fitness in foreign locations compared with resident populations from those sites (Blanquart et al., 2013) – is difficult to study in long-lived organisms through classic approaches. Yet the issue of how long-lived and broadly distributed populations persist remains a core issue at the interface of evolutionary biology and ecology with important implications for understanding how long-lived species will respond to climate change (Saenz-Romero et al., 2017). Beyond local adaptation, genetic diversity (Shaw & Etterson, 2012) and plasticity (Valladares et al., 2002a; Ramírez-Valiente et al., 2010) have also been hypothesized to be critical for persistence. Model clades can help address these questions by integrating genomic and population genetic resources, provenance trials, common gardens, and experimental ecological data.
Among species with short generation times, local adaptation has frequently been found (e.g. Joshi et al., 2001; Etterson, 2004a,b; Wright et al., 2006). Yet the extent to which long-lived organisms like oaks are locally adapted remains unclear, in part because it is difficult to test for local adaptation when experiments are shorter than generation times and frequently do not last through reproduction. Quantitative genetic methods for detecting local adaptation and rates of climate adaptation in short-lived species (Etterson & Shaw, 2001; Etterson, 2004a; Shaw & Etterson, 2012) are not well suited to trees. It is also difficult to manage the biotic environment sufficiently or to represent long-term environmental conditions within short-term experiments. However, provenance trials and field tests of a variety of tree species reveal moderate to considerable variation among populations in phenology and functional traits (Rehfeldt et al., 2002, 2006; Chuine et al., 2006), and performance across climatic gradients, including in oaks (Alberto et al., 2013; Saenz-Romero et al., 2017). These findings highlight the relevance of the question for trees. Given the ecological significance of the oaks, determining the extent to which they are narrowly or broadly adapted to climate remains an open question and is critical to developing conservation strategies in the face of climate change. I hypothesize, based on a series of studies within the live oaks, as well as various other oak species, that local adaptation occurs but is diffuse because high genetic variation is maintained within local populations and that plasticity also plays a critical role in long-term persistence.
3. Should we expect local adaptation?
Janzen (1985) posited that organisms found in the tropical dry forest of Guanacaste, Costa Rica, have largely evolved elsewhere and then expanded their ranges, ‘fitting’ into the dry forest ecosystem. He argued ‘virtually no evolution has occurred (locally) in Santa Rosa’. We used a series of reciprocal transplant experiments to test for local adaptation in the tropical live oak, Q. oleoides, which spans a range of precipitation regimes, all of which fall within the classification of seasonally dry tropics. We set up experimental gardens across two ends of a precipitation gradient, which follows elevation up the slopes of the Rincón de la Vieja mountain in northwestern Costa Rica, the adjacent lowland area of Santa Rosa National Park and in the driest part of the species range in southern Honduras across the Nicaraguan Depression (Cavender-Bares & Ramírez-Valiente, 2017); the Nicaraguan Depression is an important barrier to gene flow in oaks generally (Rodríguez-Correa et al., 2015), and separates the southernmost Q. oleoides population from the rest of its range (Cavender-Bares et al., 2011). The Costa Rican and Honduran populations are estimated to have diverged 1.9 Ma (1.0–3.1 Ma; Cavender-Bares et al., 2015). In four separate experiments, where both seeds or seedlings from known mothers were planted in a random block design (Center, 2015; Deacon & Cavender-Bares, 2015; Center et al., 2016; Ramírez-Valiente et al., 2017), we found no evidence of local adaptation at either early germination stages or after multiple years of growth across major precipitation gradients. Rather, all populations tended to perform better in climates with less severe dry seasons (Center, 2015; Deacon & Cavender-Bares, 2015; Cavender-Bares & Ramírez-Valiente, 2017; Ramírez-Valiente et al., 2017). Large-scale field experiments with Quercus petraea populations in Europe have revealed relatively modest shifts in growth and performance across climatic gradients, in contrast to what would be expected if populations were highly locally adapted (Saenz-Romero et al., 2017).
4. Adaptive differentiation in physiological function
Linking genetically based physiological tolerances of species (Koehler et al., 2012; Ramírez-Valiente & Cavender-Bares, 2017; Ramírez-Valiente et al., 2018) or known functional genes (Knight et al., 2006; Homolka et al., 2013; Gugger et al., 2016; Sork et al., 2016b) to their climatic distributions are alternative approaches to understanding adaptation to climate. Such approaches are important in predicting future distributions of species under changing climatic conditions and an active area of research. A series of recent studies have revealed genes and gene regions under selection in response to climate (Platt et al., 2015; Gugger et al., 2016, 2017; Sork et al., 2016b).
We tested for adaptive differentiation in response to low-temperature stress within and across Virentes species, which was hypothesized given their broad latitudinal distribution. Live oaks are vulnerable to freezing and occur only in climates where winters are fairly mild or absent (Miller & Lamb, 1985; Nixon, 1985; Nixon & Muller, 1997; Cavender-Bares et al., 2015). Nevertheless, three species occupy climatic regions where subzero temperatures are frequent. Given that live oaks remain active during winter, their living and nonliving tissues are subject to chilling and freezing. In a series of controlled experiments, we tested the extent to which populations at different latitudes within species are differentially adapted to chilling and freezing stress (Cavender-Bares, 2007; Cavender-Bares et al., 2011, 2015; Koehler et al., 2012). Chilling temperatures decrease enzymatic activity and metabolic rates and impair cellular transport due to reduced membrane fluidity, whereas freezing can cause intracellular ice formation that perforates membranes and ruptures cells. Freezing also causes extracellular ice formation, which may lead to cell membrane damage and dehydration stress (Fujikawa & Kuroda, 2000; Cavender-Bares, 2005). The ability to cold acclimate – that is, undergo morphological changes (including in cell wall and membrane structure) that protect against freezing damage – is also thought to be adaptive to freezing environments (Cavender-Bares, 2005; Janska et al., 2010). These changes have long been hypothesized to impose physiological costs to the plant, ultimately leading to a trade-off between the degree of cold tolerance and growth and reproductive rates (MacArthur, 1972; Loehle, 1998), although the mechanisms underlying this trade-off may be complex (Savage & Cavender-Bares, 2013). Across maternal families in all species within the Virentes, we found evidence for an evolved trade-off between freezing tolerance and growth rate, such that the maternal families from warmer latitudes within and across species showed faster growth rates but lower freezing tolerance than the maternal families from colder latitudes (Koehler et al., 2012; Fig. 5a,c,e).
In relation to drought stress, we also found variation among populations associated with climates of origin within Q. oleoides, despite our lack of direct evidence for local adaptation. Variation in the length and severity of the dry season results in contrasting selection pressures across precipitation gradients in seasonally dry tropical forests in Honduras and Costa Rica. An evolutionary trade-off between drought avoidance and drought tolerance was found in source populations across the gradient (Fig. 5d,e,f; Ramírez-Valiente & Cavender-Bares, 2017). Seedling leaves sourced from the driest sites in southern Honduras have evolved toward deciduousness, tending to abscise after prolonged experimental drought rather than osmotically adjusting to tolerate dry conditions (Ramírez-Valiente & Cavender-Bares, 2017). By contrast, seedlings sourced from the wettest populations, where the dry season incurs some rainfall even in the driest months, tend to increase the osmotic concentration of their leaves when exposed to prolonged drought, dropping their turgor loss point and increasing their drought tolerance (Fig. 5e). The wettest populations also have lower specific leaf area (SLA), which increases their drought tolerance (Fig. 5d). For these populations, it apparently pays to tolerate drought and continue gas exchange during the dry season. Tests for selection in a range of leaf morphological and physiological traits showed evidence for adaptation across precipitation gradients (Ramírez-Valiente et al., 2018). In the same experiments, seedlings exhibited plastic responses in SLA to seasonal changes in water availability and differences among garden sites, showing lower SLA in the dry season and in drier sites (Center, 2015; Ramírez-Valiente et al., 2017). Phenotypic selection analyses using aster models, which incorporate both survival and growth components of fitness (Shaw et al., 2008), revealed that, overall, seedlings with lower SLA and higher integrated water use efficiency (δ13C) had significant fitness advantages in these gardens, particularly in the dry season (Center, 2015). We also found that survival and growth rate tend to be negatively correlated across families, consistent with the hypothesis that drought tolerant individuals tend to have slower growth rates (Fig. 6b). Long-term studies that can test both for adaptation to distinct climatic regimes and identify the functional traits and genetic mechanisms that underlie these adaptations in ecologically important and long-lived species will be important in understanding ecosystem responses to climate change.
V. How do we reconcile evidence for adaptive evolution with niche conservatism and long-term stasis?
Evidence for selection and adaptive differentiation implies evolvability within the oaks, and hence lack of evolutionary stasis. Yet other evidence indicates niche conservatism – the tendency of organisms to establish and persist in environments to which they are already well adapted (Ackerly, 2003) – a widespread phenomenon in biology (Crisp et al., 2009; Wiens et al., 2010). Despite the ecological diversity and convergence in functional traits and niches found within the oaks (Cavender-Bares et al., 2004a, 2018; Hipp et al., 2018), when they are examined within the context of broad phylogenetic scales they show phylogenetic trait and niche conservatism (Cavender-Bares et al., 2006). Suites of shared derived characters are maintained throughout the oaks (Nixon, 1989; Oh & Manos, 2008) that restrict them to some environments and exclude them from others, either because they lack the physiological tolerances of those environments or they are not competitive within them. At larger spatial extents and when analyses are conducted at broad phylogenetic scales, oaks cluster within similar habitats and are excluded from wetlands and many grasslands (Cavender-Bares et al., 2006) or from forests with high annual precipitation levels or low mean annual temperature (Cavender-Bares et al., 2018).
Conservatism in various functional traits of oaks is apparent. Across 27 oak species from a range of geographic regions and habitats, the chemical composition of leaves derived from spectral reflectance signatures, as well as large regions of their leaf spectral profiles, are phylogenetically conserved. However, other leaf traits, such as SLA and spectral regions closely associated with photochemistry and light-harvesting pigments, are not (Fig. 7; Cavender-Bares et al., 2016b). Transitions between deciduousness and evergreenness across a densely sampled phylogeny of the American oaks reveal evolutionary conservatism but also represent important adaptive changes in response to climate. While transitions in leaf habit occurred multiple times in the oaks, associated with warmer minimum temperatures and lower seasonality, they tended to occur infrequently – 0.012 changes per million years (0.008–0.017; assuming a deciduous ancestor), increasing to 0.024 (0.020–0.032) changes per million years, once the oaks radiated in Mexico (Hipp et al., 2018). Thus, whereas phenological traits, such as the degree and timing of leaf abscission, appear to vary among populations within a single species (Cavender-Bares, 2007; Ramírez-Valiente & Cavender-Bares, 2017), major transitions in leaf habit do not occur frequently, although the rate of change can vary. Compared with plants globally (Wright et al., 2004), leaf lifespan in the oaks shows a relatively limited range of variation (Cavender-Bares et al., 2004b, 2005). Nevertheless, even small evolutionary changes within this limited range (Fallon & Cavender-Bares, 2018) may be critical to adaptive differentiation and persistence in novel and changing environments.
1. Leaf lifespan and phenology – flexible traits?
Riedl (1978) posited that for lineages to evolve, some areas of the lineage's architecture and developmental processes must be conserved such that major structures remain coupled, while other components could be flexible. Areas of flexibility allow for adaptations that do not break primary structure–function relationships (Wagner & Laubichler, 2004). As discussed earlier, whereas transitions in leaf habit are relatively infrequent in the oaks, they have occurred repeatedly and correspond to shifts in climatic niche. Continuous leaf traits associated with leaf lifespan and phenology, including the timing of leaf abscission and SLA, appear to be relatively flexible both in terms of their plasticity (Cavender-Bares, 2007; Firmat et al., 2017; Ramírez-Valiente et al., 2017) and in their ability to evolve (Fig. 5d–f), in a manner that appears critical for survival in and adaptation to novel or changing climates (Cavender-Bares & Holbrook, 2001; Cavender-Bares et al., 2004a; Cavender-Bares, 2007; Center, 2015; Ramírez-Valiente & Cavender-Bares, 2017; Fallon & Cavender-Bares, 2018; Hipp et al., 2018; Ramírez-Valiente et al., 2018). Flexibility in these leaf traits, even within a limited range, may thus be important in the long-term persistence of the oaks across varying environments. In other words, the evolvability of leaf traits in oaks may have enabled niche shifts across a wide range of climates, but these shifts were not rapid, and the range of variation is constrained.
VI. High plasticity and within-population genetic variation contribute to population persistence
Local adaptation and adaptive differentiation are not the only mechanisms that allow plants to occupy broad habitats and variable environments. In fact, local adaptation can reduce important genetic variation (Gharehaghaji et al., 2017). Long-lived trees that span broad geographic ranges must cope with highly variable climatic conditions, and selective pressures on growth or stress tolerance vary through space and time. A significant number of studies on both European and American oak species have found high levels of plasticity and evidence for adaptive plasticity in response to environmental variation, including temperature (Lo Gullo & Salleo, 1993; Cavender-Bares, 2007; Koehler et al., 2012), water availability (Pardos et al., 2005; Cavender-Bares et al., 2007; Barbeta et al., 2013), and light (Cavender-Bares et al., 2000; Balaguer et al., 2001; Valladares et al., 2002b; Aranda et al., 2005; Rubio De Casas et al., 2007). In Quercus petreae populations planted across Europe, considerable phenotypic plasticity in responses to variation in climate was observed, allowing populations to maintain similar growth in contrasting climates (Saenz-Romero et al., 2017).
Findings in broadly distributed Virentes species indicate that a resilient response to climate change occurs at a population level through a combination of adaptive plasticity (Ramírez-Valiente & Cavender-Bares, 2017), adaptive differentiation (Ramírez-Valiente et al., 2018), discussed earlier, and maintenance of standing genetic variation. Genetic diversity provides flexibility that ensures survival of at least some individuals during extreme events, buffering the species against extinction (Meireles et al., 2017). Meireles et al. (2017) found that evolution has favored genetic diversity through balancing selection in HOS1, a critical gene that modulates cold and freezing response by negatively regulating ICE1, a key gene in the cold acclimation pathway. Other lines of evidence also indicate that high genetic diversity is maintained in oak populations and may be more important than local adaptation in long-term persistence: the isolated Costa Rica population of Q. oleoides harbors almost as much neutral genetic diversity as does the rest of the range (Cavender-Bares et al., 2011). In common gardens, we also found high variation in fitness within families and within populations and high genetic variation in integrated water use efficiency (δ13C) within populations from across the distribution of the species (Center, 2015).
Within the range of Q. oleoides, precipitation varies strongly across local elevation gradients (Deacon & Cavender-Bares, 2015), throughout the species distribution (Ramírez-Valiente et al., 2017), and over time (Folan et al., 1983; Roy et al., 1996; Haug et al., 2001). Maintenance of high genetic diversity in alleles adaptive for more or less severe dry seasons may promote long-term persistence if contrasting alleles are associated with trade-offs between drought tolerance and growth rate and if selection pressures shift with life stage (Fig. 6). Evidence for the latter is linked to increasing rooting depth with life stage in oaks generally (Cavender-Bares & Bazzaz, 2000), indicating that mature trees typically have greater access to deep water reserves during drought than seedlings do, a pattern found in Q. oleoides during the dry season in Guanacaste, Costa Rica (Fig. 6a). Mature trees may thus be buffered from climatic fluctuations that impose strong selection on seedlings. If there are trade-offs between stress tolerance and growth efficiency that shift fitness advantages under contrasting levels of dry-season severity, balancing selection may maintain alleles for both strategies provided that alleles confer different tolerances and that seedlings are more susceptible to drought damage than adults are.
VII. Emerging technologies for tracking functional change
A final advantage of emphasizing ecological dominants as model clades is that their large size makes them amenable to novel methods for detecting changes in functional traits (Cavender-Bares et al., 2017; Schweiger et al., 2018) that can be applied with high frequency at large spatial scales. Detecting changes at the canopy scale in an era of global change is increasingly important to manage and protect ecosystem services (Jetz et al., 2016). The large canopy size of oak trees makes their detection by remote sensing possible. At the leaf level, oak species and lineages can be differentiated spectrally, including genetically based phenotypic differences among populations (Cavender-Bares et al., 2016b). Physiological functions of individual trees and ecosystem properties can both be detected in this manner (Gamon et al., 1990, 1995; Gamon & Qiu, 1999; Moya et al., 2001; Flexas et al., 2002; Freedman et al., 2002; Asner et al., 2010; Asner & Martin, 2011; Cavender-Bares et al., 2017). These advances are promising for detecting phenotypic variation, functional changes, health, and diversity of trees globally (Pontius et al., 2005, 2008; Pontius & Hallett, 2014; Jetz et al., 2016) and may also advance studies of adaptive change (Yamasaki et al., 2017). Remote-sensing approaches are likely the best option for detecting evolutionary legacy effects – that is, divergent ecosystem functions in similar environments that are a consequence of ancient biogeographic history and trait conservatism. Despite their current abundance, oaks are under threat from the increasing prevalence of oak wilt, sudden oak death, a range of other exotic pests and pathogens, and global change. If left unchecked, ecosystem function and services from forests in North America and Mesoamerica will be diminished, as they have been with losses of other forest trees (Juzwik et al., 2011).
VIII. Conclusions
Integrating ecology and evolution at multiple biological scales within a single lineage allows new insights to be generated at the interface of these fields. Interest in oaks as a model clade has led to considerable ecological, phylogenetic, and genomic data. Given that they are often ecological dominants, discoveries at the level of the genome will be relevant at the ecosystem level and can inform management in the face of threats from global change (Gailing et al., 2009; Gugger et al., 2016; Sork et al., 2016b). More broadly, focal clades are likely to promote integration across disciplines. From the oaks, several insights have emerged through this kind of integration. First, they provide an important example of how the process of diversification is critical to understanding community assembly. Often, the processes of speciation and extinction are considered far removed from the processes involved in the assembly of species into local communities, but the legacy of sympatric parallel adaptive radiation continues to influence the assembly of oak communities today. At the same time, sympatric parallel diversification may have depended on the capacity of the oaks to facilitate colonization of and coexistence with distant relatives throughout evolution, highlighting the inextricable linkages between ecological and evolutionary processes. The biogeographic history of the oaks and their conserved functional traits, at least at some evolutionary scales, influence ecosystem functions and services that are threatened today by multiple drivers of global change. Yet, adaptive differentiation in physiological function and environmental tolerances is apparent whenever it is tested for. Interspecific gene flow may contribute to adaptation and to the maintenance of high genetic diversity within populations. Maintenance of high genetic variation and evolvability of critical functional traits, coupled with plastic variation, are likely mechanisms that contribute to long-term species persistence more than adaptation to highly local conditions does.
I highlight several important areas for continued investigation. In particular, the nature and extent of coexistence mechanisms – such as reduced density-dependent mortality when distant relatives in the same genus co-occur, facilitation by shared microbial communities, and reduced competition through niche partitioning – will require experimentation. As a model clade, oaks highlight fundamental questions concerning the role of introgression in shaping community assembly, community structure, and the transfer of adaptive alleles that contribute to local adaptation and the ability to colonize new environments. Much remains to be learned about the extent of location adaptation in oaks, and in trees and long-lived species generally. Evidence suggests the possible role of plasticity and evolvability of leaf phenology, leaf lifespan, and associated hydraulic traits as areas of flexibility that allow adaptation to changing environments. The extent to which shifts in these traits influence survival in novel climates is a critical area for continued study. Finally, the ecosystem consequences of population-level variation and the prevalence and strength of evolutionary legacy effects remain largely unexamined. The role of historical processes in ecosystem function and the evolutionary mechanisms that contribute to long-term persistence of populations in the face of changing environments are central questions at the interface of ecology and evolution that have implications for management under global change and that model clades can address.
Acknowledgements
I would like to thank Scott Lanyon for first introducing me to the concept of model clades. I also wish to thank Rémy Petit, David Ackerly, an anonymous reviewer, and members of my lab who provided insights and useful feedback on the manuscript or technical assistance, including Shan Kothari, Beth Fallon, José Eduardo Meireles, Jesús Pinto-Ledezma and Anna Schweiger. Finally, I wish to thank a number of individuals, who helped me gain critical insights or provided information or other assistance: Charles Cannon, James Cavender, Nicole Cavender, Kent Cavender-Bares, Alyson Center, Nicholas Deacon, Deren Eaton, Julie Etterson, Antonio González-Rodríguez, Paul Gugger, N. Michelle Holbrook, Andrew Hipp, Diana Jerome, Paul Manos, the late George Pilz, Ruth Shaw, José Ramírez-Valiente, Jeanne Romero-Severson, Jorge Soberón, Pamela Soltis, Victoria Sork, Murphy Westwood, and the late John Tucker. This work was supported by NSF DEB 1146380 and IOS 0843665, NSF DEB-1342872 and NSF/NASA DEB-1342872.
